Hybrid allele-specific ChIP-seq analysis identifies variation in brassinosteroid-responsive transcription factor binding linked to traits in maize
Abstract Background Genetic variation in regulatory sequences that alter transcription factor (TF) binding is a major cause of phenotypic diversity. Brassinosteroid is a growth hormone that has major effects on plant phenotypes. Genetic variation in brassinosteroid-responsive cis-elements likely con...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
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BMC
2023-05-01
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| Series: | Genome Biology |
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| Online Access: | https://doi.org/10.1186/s13059-023-02909-w |
| _version_ | 1797827514254491648 |
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| author | Thomas Hartwig Michael Banf Gisele Passaia Prietsch Jia-Ying Zhu Isabel Mora-Ramírez Jos H. M. Schippers Samantha J. Snodgrass Arun S. Seetharam Bruno Huettel Judith M. Kolkman Jinliang Yang Julia Engelhorn Zhi-Yong Wang |
| author_facet | Thomas Hartwig Michael Banf Gisele Passaia Prietsch Jia-Ying Zhu Isabel Mora-Ramírez Jos H. M. Schippers Samantha J. Snodgrass Arun S. Seetharam Bruno Huettel Judith M. Kolkman Jinliang Yang Julia Engelhorn Zhi-Yong Wang |
| author_sort | Thomas Hartwig |
| collection | DOAJ |
| description | Abstract Background Genetic variation in regulatory sequences that alter transcription factor (TF) binding is a major cause of phenotypic diversity. Brassinosteroid is a growth hormone that has major effects on plant phenotypes. Genetic variation in brassinosteroid-responsive cis-elements likely contributes to trait variation. Pinpointing such regulatory variations and quantitative genomic analysis of the variation in TF-target binding, however, remains challenging. How variation in transcriptional targets of signaling pathways such as the brassinosteroid pathway contributes to phenotypic variation is an important question to be investigated with innovative approaches. Results Here, we use a hybrid allele-specific chromatin binding sequencing (HASCh-seq) approach and identify variations in target binding of the brassinosteroid-responsive TF ZmBZR1 in maize. HASCh-seq in the B73xMo17 F1s identifies thousands of target genes of ZmBZR1. Allele-specific ZmBZR1 binding (ASB) has been observed for 18.3% of target genes and is enriched in promoter and enhancer regions. About a quarter of the ASB sites correlate with sequence variation in BZR1-binding motifs and another quarter correlate with haplotype-specific DNA methylation, suggesting that both genetic and epigenetic variations contribute to the high level of variation in ZmBZR1 occupancy. Comparison with GWAS data shows linkage of hundreds of ASB loci to important yield and disease-related traits. Conclusion Our study provides a robust method for analyzing genome-wide variations of TF occupancy and identifies genetic and epigenetic variations of the brassinosteroid response transcription network in maize. |
| first_indexed | 2024-04-09T12:49:32Z |
| format | Article |
| id | doaj.art-80a9b17e31424dfb91089093cd7cfec6 |
| institution | Directory Open Access Journal |
| issn | 1474-760X |
| language | English |
| last_indexed | 2024-04-09T12:49:32Z |
| publishDate | 2023-05-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Biology |
| spelling | doaj.art-80a9b17e31424dfb91089093cd7cfec62023-05-14T11:18:39ZengBMCGenome Biology1474-760X2023-05-0124112510.1186/s13059-023-02909-wHybrid allele-specific ChIP-seq analysis identifies variation in brassinosteroid-responsive transcription factor binding linked to traits in maizeThomas Hartwig0Michael Banf1Gisele Passaia Prietsch2Jia-Ying Zhu3Isabel Mora-Ramírez4Jos H. M. Schippers5Samantha J. Snodgrass6Arun S. Seetharam7Bruno Huettel8Judith M. Kolkman9Jinliang Yang10Julia Engelhorn11Zhi-Yong Wang12Department of Plant Biology, Carnegie Institution for ScienceDepartment of Plant Biology, Carnegie Institution for ScienceDepartment of Plant Biology, Carnegie Institution for ScienceLeibniz-Institute of Plant Genetics and Crop Plant Research (IPK) GaterslebenLeibniz-Institute of Plant Genetics and Crop Plant Research (IPK) GaterslebenLeibniz-Institute of Plant Genetics and Crop Plant Research (IPK) GaterslebenDepartment of Ecology, Evolution, and Organismal Biology, Iowa State UniversityDepartment of Ecology, Evolution, and Organismal Biology, Iowa State UniversityMax Planck Institute for Plant Breeding ResearchSchool of Integrative Plant Science, Plant Pathology and Plant-Microbe Biology Section, Cornell UniversityDepartment of Agronomy and Horticulture, University of Nebraska-LincolnHeinrich-Heine UniversityDepartment of Plant Biology, Carnegie Institution for ScienceAbstract Background Genetic variation in regulatory sequences that alter transcription factor (TF) binding is a major cause of phenotypic diversity. Brassinosteroid is a growth hormone that has major effects on plant phenotypes. Genetic variation in brassinosteroid-responsive cis-elements likely contributes to trait variation. Pinpointing such regulatory variations and quantitative genomic analysis of the variation in TF-target binding, however, remains challenging. How variation in transcriptional targets of signaling pathways such as the brassinosteroid pathway contributes to phenotypic variation is an important question to be investigated with innovative approaches. Results Here, we use a hybrid allele-specific chromatin binding sequencing (HASCh-seq) approach and identify variations in target binding of the brassinosteroid-responsive TF ZmBZR1 in maize. HASCh-seq in the B73xMo17 F1s identifies thousands of target genes of ZmBZR1. Allele-specific ZmBZR1 binding (ASB) has been observed for 18.3% of target genes and is enriched in promoter and enhancer regions. About a quarter of the ASB sites correlate with sequence variation in BZR1-binding motifs and another quarter correlate with haplotype-specific DNA methylation, suggesting that both genetic and epigenetic variations contribute to the high level of variation in ZmBZR1 occupancy. Comparison with GWAS data shows linkage of hundreds of ASB loci to important yield and disease-related traits. Conclusion Our study provides a robust method for analyzing genome-wide variations of TF occupancy and identifies genetic and epigenetic variations of the brassinosteroid response transcription network in maize.https://doi.org/10.1186/s13059-023-02909-wAllele-specificTranscription factorChIP-seqBrassinosteroidRegulatory networkFunctional variation |
| spellingShingle | Thomas Hartwig Michael Banf Gisele Passaia Prietsch Jia-Ying Zhu Isabel Mora-Ramírez Jos H. M. Schippers Samantha J. Snodgrass Arun S. Seetharam Bruno Huettel Judith M. Kolkman Jinliang Yang Julia Engelhorn Zhi-Yong Wang Hybrid allele-specific ChIP-seq analysis identifies variation in brassinosteroid-responsive transcription factor binding linked to traits in maize Genome Biology Allele-specific Transcription factor ChIP-seq Brassinosteroid Regulatory network Functional variation |
| title | Hybrid allele-specific ChIP-seq analysis identifies variation in brassinosteroid-responsive transcription factor binding linked to traits in maize |
| title_full | Hybrid allele-specific ChIP-seq analysis identifies variation in brassinosteroid-responsive transcription factor binding linked to traits in maize |
| title_fullStr | Hybrid allele-specific ChIP-seq analysis identifies variation in brassinosteroid-responsive transcription factor binding linked to traits in maize |
| title_full_unstemmed | Hybrid allele-specific ChIP-seq analysis identifies variation in brassinosteroid-responsive transcription factor binding linked to traits in maize |
| title_short | Hybrid allele-specific ChIP-seq analysis identifies variation in brassinosteroid-responsive transcription factor binding linked to traits in maize |
| title_sort | hybrid allele specific chip seq analysis identifies variation in brassinosteroid responsive transcription factor binding linked to traits in maize |
| topic | Allele-specific Transcription factor ChIP-seq Brassinosteroid Regulatory network Functional variation |
| url | https://doi.org/10.1186/s13059-023-02909-w |
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